Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

Dana A. Opulente; Abigail Leavitt LaBella; Marie Claire Harrison; John F. Wolters; Chao Liu; Yonglin Li; Jacek Kominek; Jacob L. Steenwyk; Hayley R. Stoneman; Jenna VanDenAvond; Caroline R. Miller; Quinn K. Langdon; Margarida Silva; Carla Gonçalves; Emily J. Ubbelohde; Yuanning Li; Kelly V. Buh; Martin Jarzyna; Max A. B. Haase; Carlos A. Rosa; Neža Čadež; Diego Libkind; Jeremy H. DeVirgilio; Amanda Beth Hulfachor; Cletus P. Kurtzman; José Paulo Sampaio; Paula Gonçalves; Xiaofan Zhou; Xing Xing Shen; Marizeth Groenewald; Antonis Rokas; Chris Todd Hittinger

doi:10.1126/science.adj4503

Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

Dana A. Opulente, Abigail Leavitt LaBella, Marie Claire Harrison, John F. Wolters, Chao Liu, Yonglin Li, Jacek Kominek, Jacob L. Steenwyk, Hayley R. Stoneman, Jenna VanDenAvond, Caroline R. Miller, Quinn K. Langdon, Margarida Silva, Carla Gonçalves, Emily J. Ubbelohde, Yuanning Li, Kelly V. Buh, Martin Jarzyna, Max A. B. Haase, Carlos A. RosaNeža Čadež, Diego Libkind, Jeremy H. DeVirgilio, Amanda Beth Hulfachor, Cletus P. Kurtzman, José Paulo Sampaio, Paula Gonçalves, Xiaofan Zhou, Xing Xing Shen, Marizeth Groenewald, Antonis Rokas, Chris Todd Hittinger

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

Abstract

Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.

Original language	English
Article number	eadj4503
Journal	Science
Volume	384
Issue number	6694
DOIs	https://doi.org/10.1126/science.adj4503
Publication status	Published - 26 Apr 2024

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10.1126/science.adj4503

Cite this

Opulente, D. A., LaBella, A. L., Harrison, M. C., Wolters, J. F., Liu, C., Li, Y., Kominek, J., Steenwyk, J. L., Stoneman, H. R., VanDenAvond, J., Miller, C. R., Langdon, Q. K., Silva, M., Gonçalves, C., Ubbelohde, E. J., Li, Y., Buh, K. V., Jarzyna, M., Haase, M. A. B., ... Hittinger, C. T. (2024). Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts. Science, 384(6694), Article eadj4503. https://doi.org/10.1126/science.adj4503

@article{fd2aa1c7d79a4112ae5866fa5af1850d,

title = "Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts",

abstract = "Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.",

author = "Opulente, {Dana A.} and LaBella, {Abigail Leavitt} and Harrison, {Marie Claire} and Wolters, {John F.} and Chao Liu and Yonglin Li and Jacek Kominek and Steenwyk, {Jacob L.} and Stoneman, {Hayley R.} and Jenna VanDenAvond and Miller, {Caroline R.} and Langdon, {Quinn K.} and Margarida Silva and Carla Gon{\c c}alves and Ubbelohde, {Emily J.} and Yuanning Li and Buh, {Kelly V.} and Martin Jarzyna and Haase, {Max A. B.} and Rosa, {Carlos A.} and Ne{\v z}a {\v C}ade{\v z} and Diego Libkind and DeVirgilio, {Jeremy H.} and Hulfachor, {Amanda Beth} and Kurtzman, {Cletus P.} and Sampaio, {Jos{\'e} Paulo} and Paula Gon{\c c}alves and Xiaofan Zhou and Shen, {Xing Xing} and Marizeth Groenewald and Antonis Rokas and Hittinger, {Chris Todd}",

note = "Funding Information: This study was supported by National Science Foundation (NSF) grant DEB-1442148 (C.T.H.); NSF grant DEB-2110403 (C.T.H.); NSF grant DEB-1442113 (A.R.); NSF grant DEB-2110404 (A.R.); in part by DOE Great Lakes Bioenergy Research Center, funded by BER Office of Science grant DE-SC0018409 (C.T.H.); USDA National Institute of Food and Agriculture Hatch projects 1020204 and 7005101 (C.T.H.); an H. I. Romnes Faculty Fellow, supported by the Office of the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin Alumni Research Foundation (C.T.H.); National Institutes of Health (NIH), National Institute of Allergy and Infectious Diseases (NIAID) grant R56 AI146096 (A.R.); NIH, NIAID grant R01 AI153356 (A.R.); the Burroughs Wellcome Fund (A.R.); National Key R&D Program of China grant 2022YFD1401600 (X.-X.S.); National Science Foundation for Distinguished Young Scholars of Zhejiang Province grant LR23C140001 (X.-X.S.); Fundamental Research Funds for the Central Universities grant 226-2023-00021 (X.-X.S.); NIH grant T32 HG002760-16 (J.F.W.); NSF grant Postdoctoral Research Fellowship in Biology 1907278 (J.F.W.); the Howard Hughes Medical Institute through the James H. Gilliam Fellowships for Advanced Study program (J.L.S. and A.R.); NSF Graduate Research Fellowship grant DGE-1256259 (Q.K.L.); Predoctoral Training Program in Genetics, funded by the NIH grant 5T32GM007133 (Q.K.L.); Slovenian Research Agency grant P4\u20130116 (N.\u010C.); Slovenian Research Agency grant MRIC-UL ZIM, IP-0510 (N.\u010C.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant UIDB/04378/2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant LA/P/0140/ 2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/0604/2021 (C.G.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/1100/2020 (P.G.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico - Brazil CNPq grant 408733/2021 (C.A.R.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico, Brazil CNPq grant 406564/2022-1, \u201CINCT Yeasts: Biodiversity, preservation and biotechnological innovation\u201D (C.A.R.); MINCyT grant PICT-2020-SERIE A-00226 (D.L.); CONICET grant PIP 11220200102948CO (D.L.); and UNComahue grant 04/B247 (D.L.). J.L.S. is a Howard Hughes Medical Institute Awardee of the Life Sciences Research Foundation. Funding Information: We thank L. C. Horianopoulos, K. J. Fisher, L. Sun, D. J. Krause, K. T. David, C. M. Chavez, D. C. Rinker, T. K. Sato, and Hittinger laboratory and Rokas laboratory members for helpful discussions; B. Robbertse and C. Schoch for coordinating GenBank taxonomy; the yeast community for publicly depositing taxonomic type strains; the University of Wisconsin Biotechnology Center DNA Sequencing Facility (Research Resource Identifier, RRID:SCR_017759) for providing DNA sequencing facilities and services; Wisconsin Energy Institute staff for computational support; and the Center for High-Throughput Computing at the University of Wisconsin\u2013Madison (https://chtc.cs.wisc.edu/). This work was performed in part using resources contained within the Advanced Computing Center for Research and Education at Vanderbilt University in Nashville, TN. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture (USDA). USDA is an equal opportunity provider and employer. Funding: This study was supported by National Science Foundation (NSF) grant DEB-1442148 (C.T.H.); NSF grant DEB-2110403 (C.T.H.); NSF grant DEB-1442113 (A.R.); NSF grant DEB-2110404 (A.R.); in part by DOE Great Lakes Bioenergy Research Center, funded by BER Office of Science grant DE-SC0018409 (C.T.H.); USDA National Institute of Food and Agriculture Hatch projects 1020204 and 7005101 (C.T.H.); an H. I. Romnes Faculty Fellow, supported by the Office of the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin Alumni Research Foundation (C.T.H.); National Institutes of Health (NIH), National Institute of Allergy and Infectious Diseases (NIAID) grant R56 AI146096 (A.R.); NIH, NIAID grant R01 AI153356 (A.R.); the Burroughs Wellcome Fund (A.R.); National Key R&D Program of China grant 2022YFD1401600 (X.-X.S.); National Science Foundation for Distinguished Young Scholars of Zhejiang Province grant LR23C140001 (X.-X.S.); Fundamental Research Funds for the Central Universities grant 226-2023-00021 (X.-X.S.); NIH grant T32 HG002760-16 (J.F.W.); NSF grant Postdoctoral Research Fellowship in Biology 1907278 (J.F.W.); the Howard Hughes Medical Institute through the James H. Gilliam Fellowships for Advanced Study program (J.L.S. and A.R.); NSF Graduate Research Fellowship grant DGE-1256259 (Q.K.L.); Predoctoral Training Program in Genetics, funded by the NIH grant 5T32GM007133 (Q.K.L.); Slovenian Research Agency grant P4\u20130116 (N.\u010C.); Slovenian Research Agency grant MRIC-UL ZIM, IP-0510 (N.\u010C.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant UIDB/04378/2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant LA/P/0140/ 2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/0604/2021 (C.G.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/1100/2020 (P.G.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico - Brazil CNPq grant 408733/2021 (C.A.R.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico, Brazil CNPq grant 406564/2022-1, \u201CINCT Yeasts: Biodiversity, preservation and biotechnological innovation\u201D (C.A.R.); MINCyT grant PICT-2020-SERIE A-00226 (D.L.); CONICET grant PIP 11220200102948CO (D.L.); and UNComahue grant 04/B247 (D.L.). J.L.S. is a Howard Hughes Medical Institute Awardee of the Life Sciences Research Foundation. Author contributions: D.A.O. designed and implemented research, led phenotypic data collection, led genome sequencing, performed computational analyses and statistical analyses, managed data, and prepared figures. A.L.L. designed and implemented computational analyses, managed data, and prepared figures. M.C.H. designed and implemented machine learning analyses. J.F.W. designed and implemented genome filtering and data curation pipelines. J.K. and J.L.S. conducted data curation and filtering. X.-X.S. led the phylogenomic analyses with C.L. and Yu.L. X.Z. led the annotation of genomes with Yo.L. D.A.O., H.R.S., J.V., C.R.M., Q.K.L., E.J.U., and A.B.H. phenotyped and sequenced strains. M.S. and C.G. performed fructophilic phenotyping experiments. D.A.O., K.V.B., M.J., M.A.B.H., Q.K.L., C.A.R., N.\u010C., D.L., C.P.K., M.G., and C.T.H. provided yeast strains. J.H.D., A.B.H., C.P.K., and M.G. curated and organized strains and metadata. J.P.S. contributed resources to fructophilic phenotyping experiments. P.G. supervised fructophilic phenotyping experiments. C.P.K. and M.G. led the taxonomy. D.A.O. and A.L.L. cowrote the manuscript with contributions from M.-C.H., J.F.W., J.K., J.L.S., C.G., P.G., X.Z., X.-X.S., M.G., A.R., and C.T.H. A.R. and C.T.H. edited the manuscript. C.P.K., A.R., and C.T.H. designed the research, obtained funding, and supervised the project. All authors provided comments and input and approved the manuscript. Competing interests: J.L.S. was a scientific adviser for WittGen Biotechnologies and is an adviser for ForensisGroup, Inc. A.R. is a scientific consultant for LifeMine Therapeutics, Inc. The authors declare no other competing interests. Data and materials availability: All genome sequence assemblies and raw sequencing data have been deposited in GenBank under the accessions noted in data S1. All other data, including data on growth on different carbon and nitrogen sources and isolation environment data, have been deposited in Figshare (42). All code has been deposited in GitHub, available through Zenodo (92, 93), and is available in Figshare (42). Nearly all strains came from globally recognized yeast culture collections and may be ordered from the USDA (https://nrrl.ncaur.usda.gov for NRRL strains) or Westerdijk Fungal Biodiversity Institute (https:// wi.knaw.nl for CBS strains) under their respective material transfer agreements (MTAs) for publicly deposited strains; currently, NRRL only requires an MTA for strains requiring BSL-2 precautions. Strains from the Hittinger laboratory that represent candidates for novel species that have not yet been formally described or deposited at CBS or NRRL may be obtained from C.T.H. under the Uniform Biological MTA or another mutually acceptable MTA. License information: Copyright \u00A9 2024 the authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original US government works. https://www.science.org/about/science-licenses-journal-article-reuse. This article is subject to HHMI\u2019s Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the Author Accepted Manuscript (AAM) of this article can be made freely available under a CC BY 4.0 license immediately upon publication. Publisher Copyright: {\textcopyright} 2024 American Association for the Advancement of Science. All rights reserved.",

year = "2024",

month = apr,

day = "26",

doi = "10.1126/science.adj4503",

language = "English",

volume = "384",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6694",

}

Opulente, DA, LaBella, AL, Harrison, MC, Wolters, JF, Liu, C, Li, Y, Kominek, J, Steenwyk, JL, Stoneman, HR, VanDenAvond, J, Miller, CR, Langdon, QK, Silva, M , Gonçalves, C, Ubbelohde, EJ, Li, Y, Buh, KV, Jarzyna, M, Haase, MAB, Rosa, CA, Čadež, N, Libkind, D, DeVirgilio, JH, Hulfachor, AB, Kurtzman, CP, Sampaio, JP , Gonçalves, P, Zhou, X, Shen, XX, Groenewald, M, Rokas, A & Hittinger, CT 2024, 'Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts', Science, vol. 384, no. 6694, eadj4503. https://doi.org/10.1126/science.adj4503

TY - JOUR

T1 - Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

AU - Opulente, Dana A.

AU - LaBella, Abigail Leavitt

AU - Harrison, Marie Claire

AU - Wolters, John F.

AU - Liu, Chao

AU - Li, Yonglin

AU - Kominek, Jacek

AU - Steenwyk, Jacob L.

AU - Stoneman, Hayley R.

AU - VanDenAvond, Jenna

AU - Miller, Caroline R.

AU - Langdon, Quinn K.

AU - Silva, Margarida

AU - Gonçalves, Carla

AU - Ubbelohde, Emily J.

AU - Li, Yuanning

AU - Buh, Kelly V.

AU - Jarzyna, Martin

AU - Haase, Max A. B.

AU - Rosa, Carlos A.

AU - Čadež, Neža

AU - Libkind, Diego

AU - DeVirgilio, Jeremy H.

AU - Hulfachor, Amanda Beth

AU - Kurtzman, Cletus P.

AU - Sampaio, José Paulo

AU - Gonçalves, Paula

AU - Zhou, Xiaofan

AU - Shen, Xing Xing

AU - Groenewald, Marizeth

AU - Rokas, Antonis

AU - Hittinger, Chris Todd

N1 - Funding Information: This study was supported by National Science Foundation (NSF) grant DEB-1442148 (C.T.H.); NSF grant DEB-2110403 (C.T.H.); NSF grant DEB-1442113 (A.R.); NSF grant DEB-2110404 (A.R.); in part by DOE Great Lakes Bioenergy Research Center, funded by BER Office of Science grant DE-SC0018409 (C.T.H.); USDA National Institute of Food and Agriculture Hatch projects 1020204 and 7005101 (C.T.H.); an H. I. Romnes Faculty Fellow, supported by the Office of the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin Alumni Research Foundation (C.T.H.); National Institutes of Health (NIH), National Institute of Allergy and Infectious Diseases (NIAID) grant R56 AI146096 (A.R.); NIH, NIAID grant R01 AI153356 (A.R.); the Burroughs Wellcome Fund (A.R.); National Key R&D Program of China grant 2022YFD1401600 (X.-X.S.); National Science Foundation for Distinguished Young Scholars of Zhejiang Province grant LR23C140001 (X.-X.S.); Fundamental Research Funds for the Central Universities grant 226-2023-00021 (X.-X.S.); NIH grant T32 HG002760-16 (J.F.W.); NSF grant Postdoctoral Research Fellowship in Biology 1907278 (J.F.W.); the Howard Hughes Medical Institute through the James H. Gilliam Fellowships for Advanced Study program (J.L.S. and A.R.); NSF Graduate Research Fellowship grant DGE-1256259 (Q.K.L.); Predoctoral Training Program in Genetics, funded by the NIH grant 5T32GM007133 (Q.K.L.); Slovenian Research Agency grant P4\u20130116 (N.\u010C.); Slovenian Research Agency grant MRIC-UL ZIM, IP-0510 (N.\u010C.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant UIDB/04378/2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant LA/P/0140/ 2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/0604/2021 (C.G.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/1100/2020 (P.G.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico - Brazil CNPq grant 408733/2021 (C.A.R.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico, Brazil CNPq grant 406564/2022-1, \u201CINCT Yeasts: Biodiversity, preservation and biotechnological innovation\u201D (C.A.R.); MINCyT grant PICT-2020-SERIE A-00226 (D.L.); CONICET grant PIP 11220200102948CO (D.L.); and UNComahue grant 04/B247 (D.L.). J.L.S. is a Howard Hughes Medical Institute Awardee of the Life Sciences Research Foundation. Funding Information: We thank L. C. Horianopoulos, K. J. Fisher, L. Sun, D. J. Krause, K. T. David, C. M. Chavez, D. C. Rinker, T. K. Sato, and Hittinger laboratory and Rokas laboratory members for helpful discussions; B. Robbertse and C. Schoch for coordinating GenBank taxonomy; the yeast community for publicly depositing taxonomic type strains; the University of Wisconsin Biotechnology Center DNA Sequencing Facility (Research Resource Identifier, RRID:SCR_017759) for providing DNA sequencing facilities and services; Wisconsin Energy Institute staff for computational support; and the Center for High-Throughput Computing at the University of Wisconsin\u2013Madison (https://chtc.cs.wisc.edu/). This work was performed in part using resources contained within the Advanced Computing Center for Research and Education at Vanderbilt University in Nashville, TN. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture (USDA). USDA is an equal opportunity provider and employer. Funding: This study was supported by National Science Foundation (NSF) grant DEB-1442148 (C.T.H.); NSF grant DEB-2110403 (C.T.H.); NSF grant DEB-1442113 (A.R.); NSF grant DEB-2110404 (A.R.); in part by DOE Great Lakes Bioenergy Research Center, funded by BER Office of Science grant DE-SC0018409 (C.T.H.); USDA National Institute of Food and Agriculture Hatch projects 1020204 and 7005101 (C.T.H.); an H. I. Romnes Faculty Fellow, supported by the Office of the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin Alumni Research Foundation (C.T.H.); National Institutes of Health (NIH), National Institute of Allergy and Infectious Diseases (NIAID) grant R56 AI146096 (A.R.); NIH, NIAID grant R01 AI153356 (A.R.); the Burroughs Wellcome Fund (A.R.); National Key R&D Program of China grant 2022YFD1401600 (X.-X.S.); National Science Foundation for Distinguished Young Scholars of Zhejiang Province grant LR23C140001 (X.-X.S.); Fundamental Research Funds for the Central Universities grant 226-2023-00021 (X.-X.S.); NIH grant T32 HG002760-16 (J.F.W.); NSF grant Postdoctoral Research Fellowship in Biology 1907278 (J.F.W.); the Howard Hughes Medical Institute through the James H. Gilliam Fellowships for Advanced Study program (J.L.S. and A.R.); NSF Graduate Research Fellowship grant DGE-1256259 (Q.K.L.); Predoctoral Training Program in Genetics, funded by the NIH grant 5T32GM007133 (Q.K.L.); Slovenian Research Agency grant P4\u20130116 (N.\u010C.); Slovenian Research Agency grant MRIC-UL ZIM, IP-0510 (N.\u010C.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant UIDB/04378/2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant LA/P/0140/ 2020 (C.G., P.G., and J.P.S.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/0604/2021 (C.G.); Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia grant PTDC/BIA-EVL/1100/2020 (P.G.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico - Brazil CNPq grant 408733/2021 (C.A.R.); Conselho Nacional de Desenvolvimento Cient\u00EDfico e Tecnol\u00F3gico, Brazil CNPq grant 406564/2022-1, \u201CINCT Yeasts: Biodiversity, preservation and biotechnological innovation\u201D (C.A.R.); MINCyT grant PICT-2020-SERIE A-00226 (D.L.); CONICET grant PIP 11220200102948CO (D.L.); and UNComahue grant 04/B247 (D.L.). J.L.S. is a Howard Hughes Medical Institute Awardee of the Life Sciences Research Foundation. Author contributions: D.A.O. designed and implemented research, led phenotypic data collection, led genome sequencing, performed computational analyses and statistical analyses, managed data, and prepared figures. A.L.L. designed and implemented computational analyses, managed data, and prepared figures. M.C.H. designed and implemented machine learning analyses. J.F.W. designed and implemented genome filtering and data curation pipelines. J.K. and J.L.S. conducted data curation and filtering. X.-X.S. led the phylogenomic analyses with C.L. and Yu.L. X.Z. led the annotation of genomes with Yo.L. D.A.O., H.R.S., J.V., C.R.M., Q.K.L., E.J.U., and A.B.H. phenotyped and sequenced strains. M.S. and C.G. performed fructophilic phenotyping experiments. D.A.O., K.V.B., M.J., M.A.B.H., Q.K.L., C.A.R., N.\u010C., D.L., C.P.K., M.G., and C.T.H. provided yeast strains. J.H.D., A.B.H., C.P.K., and M.G. curated and organized strains and metadata. J.P.S. contributed resources to fructophilic phenotyping experiments. P.G. supervised fructophilic phenotyping experiments. C.P.K. and M.G. led the taxonomy. D.A.O. and A.L.L. cowrote the manuscript with contributions from M.-C.H., J.F.W., J.K., J.L.S., C.G., P.G., X.Z., X.-X.S., M.G., A.R., and C.T.H. A.R. and C.T.H. edited the manuscript. C.P.K., A.R., and C.T.H. designed the research, obtained funding, and supervised the project. All authors provided comments and input and approved the manuscript. Competing interests: J.L.S. was a scientific adviser for WittGen Biotechnologies and is an adviser for ForensisGroup, Inc. A.R. is a scientific consultant for LifeMine Therapeutics, Inc. The authors declare no other competing interests. Data and materials availability: All genome sequence assemblies and raw sequencing data have been deposited in GenBank under the accessions noted in data S1. All other data, including data on growth on different carbon and nitrogen sources and isolation environment data, have been deposited in Figshare (42). All code has been deposited in GitHub, available through Zenodo (92, 93), and is available in Figshare (42). Nearly all strains came from globally recognized yeast culture collections and may be ordered from the USDA (https://nrrl.ncaur.usda.gov for NRRL strains) or Westerdijk Fungal Biodiversity Institute (https:// wi.knaw.nl for CBS strains) under their respective material transfer agreements (MTAs) for publicly deposited strains; currently, NRRL only requires an MTA for strains requiring BSL-2 precautions. Strains from the Hittinger laboratory that represent candidates for novel species that have not yet been formally described or deposited at CBS or NRRL may be obtained from C.T.H. under the Uniform Biological MTA or another mutually acceptable MTA. License information: Copyright \u00A9 2024 the authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original US government works. https://www.science.org/about/science-licenses-journal-article-reuse. This article is subject to HHMI\u2019s Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the Author Accepted Manuscript (AAM) of this article can be made freely available under a CC BY 4.0 license immediately upon publication. Publisher Copyright: © 2024 American Association for the Advancement of Science. All rights reserved.

PY - 2024/4/26

Y1 - 2024/4/26

N2 - Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.

AB - Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.

UR - http://www.scopus.com/inward/record.url?scp=85191492230&partnerID=8YFLogxK

U2 - 10.1126/science.adj4503

DO - 10.1126/science.adj4503

M3 - Article

C2 - 38662846

AN - SCOPUS:85191492230

SN - 0036-8075

VL - 384

JO - Science

JF - Science

IS - 6694

M1 - eadj4503

ER -

Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

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